A new species of woolly horseshoe bat in the Rhinolophus trifoliatus species group is described from Sabah in Malaysian Borneo. Two specimens from Central and West Kalimantan, Indonesia are referred to this species. A fourth specimen from western Thailand is referable to this species but on the basis of ~10% genetic divergence at the cytochrome oxidase-I gene is described as a separate subspecies. Morphologically and acoustically the two subspecies are similar. With a forearm length of 52.90–54.70 mm, a skull length of 24.27–26.57 mm and a call frequency of 49.2–50.0 kHz, the new species overlaps in size and call frequency with the sympatric R. trifoliatus. However, it differs significantly in having a dark noseleaf and a uniformly dark brown pelage, resembling, but being intermediate in size between R. sedulus and R. luctus, which have a skull length of 18.99–20.17 and 26.35–32.07 mm, respectively. It also differs from R. trifoliatus in the shape and size of the rostral inflation. It can be distinguished from R. beddomei (forearm length 55.00–63.44 mm) and R. formosae (forearm length 53.85–62.40 mm), which are endemic to the Indian Subcontinent and Taiwan, respectively, by its relatively smaller body size. Acoustic and genetic data are included in the comparison between the species. Both character states support the conclusions based on morphology. Further surveys in intact evergreen forest together with a re-examination of museum specimens may reveal that this species is widespread in Southeast Asia.

Rhinolophus is the single extant genus in the family Rhinolophidae. With at least 87 species cur-rently recognised, it is also one of the most diverse among bat genera and is widely distributed through-out much of the Old World (Simmons, 2005; Yoshiyuki and Lim, 2005; Soisook et al ., 2008; Wu et al., 2008, 2009; Wu and Thong, 2009; Zhou et al., 2009; Taylor et al., 2012). Within the genus, the species have been arranged into several groups based mainly on morphological characters (e.g., shape of the sella, noseleaf and cranial features). This has led to differences of opinion regarding the systematics (e.g., Guillén et al., 2003). None theless, the most widely accepted and most comprehensive review of the Rhinolophidae can be found in Csorba et al. (2003).

For echolocation, all species of Rhinolophus, and the sister genus Hipposideros, use a high duty cycle, long and narrow band, constant frequency (CF) com ponent, which is adapted for the detection of fluttering insects (Kalko and Schnitzler, 1998). Recent studies of the echolocation characters of the ‘CF bats’ strongly suggest that acoustic characters are useful for species identification (Francis and Haber setzer, 1998; Francis et al., 1999; Kingston et al., 2001; Thabah et al., 2006; Soisook et al., 2008; Hughes et al., 2010; Ith et al., 2011; Taylor et al., 2012; Thong et al., 2012). Moreover, acoustic divergence within species, which may result from the isolation of populations and adaptation due to local environment, can result in genetic drift and in some cases has led to speciation (Kingston and Rossiter, 2004; Chen et al., 2009; Taylor et al., 2012).

Species in the ‘trifoliatus-group’ are characterised by the presence of a lateral lappet on each side of the base of the sella of the noseleaf. Currently, the group is widely distributed from the Indian subcon-tinent, eastwards to Southeast and eastern Asia, and is represented by five species (Csorba et al., 2003; Simmons, 2005). Until this study, three species of this group were known to occur in Southeast Asia, namely R. luctus, R. trifoliatus and R. sedulus(Francis, 2008) whilst two species, R. beddomei and R. formosae, were thought to be geographically more restricted, recorded from the Indian Subcontinent and Taiwan, respectively (Csorba et al., 2003; Simmons, 2005).

In 2010, R. beddomei was reported for the first time from Southeast Asia based on the morphological characters of a single specimen collected from evergreen forest in western Thailand (Soisook et al., 2010). However, the authors acknowledged that the smaller size of the Thai specimen and the disjunct distribution suggested that additional specimens could confirm this as a different species (Soisook et al., 2010). Fortunately, recent field surveys by a network of researchers in Southeast Asian countries using harp traps in forest habitats has provided additional material. This, combined with a re-examination of a specimen collected from Sabah in 1983 by Charles M. Francis and housed in the Natural History Museum, London makes a more thorough comparative study possible. Francis’s specimen was provisionally identified and labelled R. trifoliatus (see also Payne et al., 1985).

With a larger sample size and with acoustic and genetic data available to compare with other congeneric species, these specimens have proved to be distinct from other taxa within the group and are described here as a new species.

Etymology: The species is named in honour of Charles M. Francis, who, for many years, has contributed greatly to the taxonomic study of Southeast Asian bats. He also collected the holotype of this species from Sabah, Malaysian Borneo in 1983. The proposed English name is ‘Francis’s Woolly Horseshoe Bat’.

Ecology and conservation notes: In Borneo, the type specimen from Gunung Trus Madi in Sabah was caught in a mist net set in forest on a mountain ridge (C. M. Francis, personal communication). It was found along with seven other bat species during the expedition in 1983 (Sheldon and Francis, 1985). A second individual was captured in undisturbed evergreen forest of Maliau Basin and subsequently released. The specimens from Kalimantan were collected in undisturbed (Tanjung Puting National Park; Gunung Palung National Park), and logged evergreen forest (Nanga Tayap — specimens subsequently released), at sites where both R. sedulus and R. trifoliatus were also present (Struebig et al., 2006). In Thailand, a single specimen from Mae Nam Pha Chi was captured in a harp trap set over a seasonal streamlet surround ed by dense primary evergreen forest at an elevation of 431 m a.s.l. It was found at dawn in the same trap as Nycteris tragata, R. microglobosus, Myotis muricola, Kerivoula papillosa and Phoniscus jagorii (Soisook et al., 2010). The collection sites of Trus Madi, Tanjung Puting and, Mae Nam Pha Chi are legally protected forests, as are survey sites Maliau Basin and Gunung Palung. However, the hunting of mammals may still be a problem across this region, and is considered as major threat to wildlife.

Distribution: Rhinolophus francisi is currently known from only six records; with two records in Sabah, Malaysian Borneo; three in Indonesian Borneo (Kalimantan) and a single record in Thailand (see below). The species may be distributed more widely in these regions, but has been rarely captured despite extensive surveys. Genetic data also suggest that this species is likely to occur in Vietnam, although this needs to be confirmed.

In the family Rhinolophidae, the members of the trifoliatus clade are easily recognisable by a unique noseleaf structure and a fluffy fur. Within this group, Rhinolophus luctus is the largest species with currently six recognized subspecies, distributed from India to Bali. We investigated genetic (karyotype, mitochondrial DNA sequence) and morphological characters from a Peninsular Malaysian sample. Although the diploid number was 2n = 32 in all specimens, karyotype analysis revealed two largely different chromosomal sets, with a Y-autosome translocation present only in one of the taxa. Morphological examination revealed differences concerning size of the baculum and length of the lower toothrow. Based on these results, a new species is described [Rhinolophus luctoides] and the former subspecies distributed on the Malayan Peninsula, Rhinolophus luctus morio, is elevated to species rank, Rhinolophus morio.

In 2005, the number of recognized species of the monotypic family Rhinolophidae (horseshoe bats) was 77 (Simmons, 2005). Since then, at least 19 new species have been described on the basis of morphological differences, corroborated by molecular (12 species) and karyological (one species) data, at present resulting in a total of about 96 species (Yoshiyuki and Lim, 2005; Soisook et al., 2008; Wu et al., 2008, 2009, 2011; Zhou et al., 2009; Benda and Vallo, 2012; Taylor et al., 2012; Kerbis Peterhans et al., 2013; Patrick et al., 2013, Soisook et al., 2015). This rapid increase in species number reflects the notion that the general morphological uniformity in the genus Rhinolophus masks subtle species specific differences, which can be recognized only through detailed studies. Representative examples, where species initially have been proposed on the basis of DNA sequence divergences that were subsequently confirmed by morphological data, can be found in South Africa (Taylor et al., 2012; Jacobs et al., 2013) and South-East Asia (Patrick et al., 2013). Based on morphological features, the genus Rhinolophus is divided into 15 groups (Csorba et al., 2003). Among these, most easily recognized are the members of the R. trifoliatus group by their long, fluffy fur and a unique noseleaf structure with lateral lappets at the base of the sella. This clade, which corresponds to the subgenus Aquias Gray 1847 (Guillén-Servent et al., 2003), is distributed from the Indian subcontinent to Southeast Asia. The mem bers of the trifoliatus group are clearly distinguished by their body size. In addition to the smallsized species R. sedulus and the medium-sized R. trifoliatus, large-sized members are found throughout the whole distributional range, from Sri Lanka to Nepal on the Indian subcontinent in the west, to the southern parts of China in the east and
north, and to the Indonesian islands Java, Sumatra
and Bali in the south. The first large-sized specimen
from Java was described as R. luctus by Temminck
in 1835.

However, quite a large number of subspecies
or closely related species has been described
subsequently, which were all subsumed as subspecies
of R. luctus by Tate in 1943. A short summary
of the complicated history of this taxon can
be found in Topál and Csorba (1992). The Indian
R. beddomei, formerly a subspecies of R. luctus, was
elevated to species rank for the reason of a different
shape of the upper canine and general size differences
(Topál and Csorba, 1992). A deviating diploid
chromosome number (see below) and smaller body
size led Yoshiyuki and Harada (1995) to re-establish
the specific rank of R. formosae Sanborn, 1939.
However, there are still six different names,
which have originally been designated as names for
species, subspecies or races but are now all subsumed
under the species name Rhinolophus luctus.
Simmons (2005) accepted perniger, lanosus, spurcus
as inhabitants of the northern parts of the distributional
range, as well as luctus, morio and foetidus
as subspecies of R. luctus, whereas geminus was
considered as synonymous with luctus. The assignment
of a specimen to a certain R. luctus subspecies
can presently be done only by the sampling locality
as distinct morphological differences have not been
described.

The members of the trifoliatus clade are not only
clearly separated by morphological features from
their congeners, but also by a cytogenetic feature,
i.e., a low diploid chromosome number (2n). Typically, the genus Rhinolophus is karyologically characterized
by a high 2n with the majority of species
showing a diploid number higher than 56. Apart
from the exceptional case of R. hipposideros with
its three karyotypic variants 2n = 54, 56 and 58 (reviewed
in Volleth et al., 2013), only a small number
of species with a diploid chromosome number
smaller than 56 has been reported so far. According
to Csorba et al. (2003) they belong to four species
groups: (1) the rouxi group (R. rouxi 2n = 56, R. sinicus
2n = 36, R. thomasi 2n = 36), (2) the pearsoni
group (R. pearsoni 2n = 42 and 44, R. yunanensis
2n = 46) and (3) the euryotis group (R. rufus 2n = 40)
(Zhang, 1985; Zima et al., 1992; Rickart et al.,
1999; Gu et al., 2003; Ao et al., 2007; Mao et al.,
2007; Wu et al., 2009). The fourth group with 2n
lower than 56 is the R. trifoliatus clade.

Up to now, only conventionally stained chromosomes
of two R. luctus subspecies have been
described. A non-differentially stained karyotype
with 2n = 32, a submetacentric X and an acrocentric
Y from a single male specimen assigned to
R. l. perniger was reported by Harada et al. (1985)
from northern Thailand. From a central Thailand
province, a female specimen designated as
R. l. morio with 2n = 32 was described having
a karyotype similar to R. l. perniger, however, without
presenting a karyotype image (Hood et al.,
1988). A karyotype comprising 2n = 32 chromosomes
has also been reported for R. beddomei from
India (Naidu and Gururaj, 1984; Koubínová et al.,
2010). Further, according to the differing diploid
number of 52 (Ando et al., 1980, 1983), the former
R. luctus subspecies formosae is now treated as
a separate species (Yoshiyuki and Harada, 1995).
The only species from the trifoliatus group for
which a differentially stained karyotype has been
published is the smallest species of the clade,
R. sedulus, with a diploid number of 2n = 28 (Volleth et al., 2014).

During our chromosomal study of members of
the trifoliatus group from Peninsular Malaysia, we
were intrigued to find two distinctly different chromosomal
sets among our ‘R. luctus’ sample. Initially, the discovery of an unusual sex chromosome
system in the first specimen called for the investigation
of additional specimens. The second individual,
however, unexpectedly carried a different karyotype. In the present paper we report on morphological,
karyological and mitochondrial DNA sequence
differences found between these two cryptic rhinolophid species from Peninsular Malaysia. The results
show that two forms exist in close geographic
proximity, which according to genetic features represent
distinct species.

Etymology: The name luctoides was chosen because this species, regarding external appearance, is very similar to subspecies of R. luctus.

Habitat: Rhinolophus luctoides was found in selectively logged Dip tero carp Rain Forest at elevations higher than 600 m, 5 km NE of the Field Studies Centre (FSC) of Ulu Gombak, and in Montane Rain Forest of Gent ing Highlands and Cameron Highlands. The hab itat of the Gombak valley, where the FSC is situated, has been described in detail by Medway (1966). The surroundings of the FSC have been reported as one of the locations with the highest species richness of bats in the Old World (Sing et al., 2013).

Rhinolophus morio Gray, 1842 status revivisco

The skull dimensions of the holotype of R. morio Gray, 1842 from Singapore, deposited in the Natural History Museum London, are similar to those of the two lowland specimens collected by us in the vicinity of Kuala Lumpur (Templer Park, Rawang). Concerning the ratio of lower toothrow to mandible length, the taxon morio comes close to subspecies of R. luctus (perniger, foetidus, lanosus). However, morio differs clearly in the ratio zygomatic width to mandible length from the above mentioned subspecies. In this respect, morio resembles other genera in the trifoliatus clade, i.e. R. trifoliatus, R. sedulus and R. beddomei (Table 3). By reason of these cranial proportions and the characteristic karyotype with the unique Y-autosomal translocation (see below), we elevate the taxon morio to species rank (Rhinolophus morio stat. rev.).

Paul[in]a's Limestone Rat Saxatilomys paulinaeMusser et al., 2005 was first discovered by Musser etal. (2005) based on specimens from the Khammouane Limestone National Biodiversity Conservation Area (NBCA) in Khammouane Province in central Lao People's Democratic Republic (PDR). This tower karst landscape is part of the Central Indochina Limestone massif, which extends eastward into north-central Vietnam in Quang Binh and Quang Tri Provinces.

New information

In April 2014, we conducted a rodent survey and collected four (4) whole specimens of Saxatilomys paulinae in Quang Binh province. This is the first record of Saxatilomys paulinae in Vietnam. External and craniodental characteristics of all specimens clearly exhibit the characters of Saxatilomys paulinae as described in Musser et al. (2005)​. The rats are of medium size (HB: 160.3 ± 2.03 mm, T: 192.3 ± 6.69 mm) with some specific morpological characteristics. The external and craniodental measurement of the specimens from Vietnam tend to be larger than those of specimens from Lao. However, this needs to be verified by more studies in future. The habitat of Saxatilomys paulinae in Vietnam is characterized by complicated terrain comprising low karst towers (around 400 m) with steep slopes covered under limestone humid evergreen forest. The forest has been affected by selected timber logging in the past, but still has a complex 4-layer structure. The population of Saxatilomys paulinae in Vietnam is threatened by rodent trapping/snaring and habitat disturbance. More status surveys should be conducted to assess the species distributional range and its population status for undertaking relevant conservation measures.

Simple comparison of external and craniodental measurement of specimens from Vietnam with those of specimens from Lao indicates that specimens from Vietnam are generally larger than specimens from Lao (Table 1​). However, due to very small number of specimens examined, this needs to be verified by more studies in future.

In Lao, Saxatilomys paulinae was reported to inhabit steep rocky slopes with large limestone boulders covered in heavily degraded deciduous forest mixed with scrub and bamboo at the base of the surrounding massive karst (Musser et al. 2005). Vietnam's population of Saxatilomys paulinae was found in rocky slopes with large limestone boulders, under the limestone humid evergreen forest which is different from the deciduous forest type in Lao. This indicates Saxatilomys paulinae can tolerate different limestone forest habitats existing in the Central Indochina Limestone landscape.

Before this study, Saxatilomys paulinae was recorded only in the Phoun Hin Poun NBCA in Khammuoane province of Lao (Musser et al. 2005). Our records of Saxatilomys paulinae in Quang Binh province expand global distribution range of this species into Vietnam's part of Central Indochina Limestone for about 100 km east-ward. However, the range of the species distribution remains restricted by only five known localities (four localities in Lao and one locality in Vietnam), while trapping and habitat disturbance remain as current threats to the species survival. More surveys need to be conducted to assess the species distributional range and the status of its populations for undertaking relevant conservation measures.

It is interesting that both Saxatilomys paulinae and Laonastes aenigmamus share the same limestone forest habitat in Central Indochina Limestone. The Laonastes aenigmamus is the only surviving member of the otherwise extinct rodent family Diatomyidae, that was formerly believed to have been extinct for more than 11 million years (Dawson et al. 2006). Both species are currently known only from few localities in Central Indochina Limestone. This again indicates high importance of the Central Indochina Limestone for the global biodiversity conservation.

Fig. 6. Views of the cranium and dentary of Saxatilomys paulinae (holotype, BMNH 2000.292) from Lao PDR.
Note the triangular postorbital region in S. paulinae (vase-shaped in Niviventer tenaster), the narrower incisive foramina, the longer palate projecting beyond molar rows to form a platform, the diverging molar rows, the wider zygomatic plate, and the pattern formed by the squamosal root of the zygomatic arch relative to the temporal ridge (also see fig. 8).

Saxatilomys paulinae, a new genus and species of murid rodent in the Dacnomys Division is described. It is based on two whole specimens and 14 individuals represented by fragments recovered from owl pellets. The samples come from the Khammouan Limestone National Biodiversity Conservation Area in Khammouan Province in central Lao PDR. This tower karst landscape is part of the Quy Dat limestone massif, which extends eastward into north-central Vietnam (Binh Tri Thien Province). The new genus and species is morphologically (and probably phylogenetically) allied to species of Niviventer and Chiromyscus, which are also members of the Dacnomys Division, but its semispinous dark gray upperparts, dark frosted gray underparts, large, extremely bulbous footpads, and a combination of derived and primitive cranial and dental traits exclude it from membership in Niviventer, Chiromyscus, or any other described genus of Indo-malayan murid. The new species is likely petricolous, and is part of a small but unique community of small nonvolant mammals containing the petricolous gymnure, Hylomys megalotis, and hystricognath, Laonastes aenigmamus. All three species have been collected only in forested, rocky habitats of the Khammouan Limestone, but comparable environments in the adjacent Vietnamese portion of the Quy Dat limestone massif may harbor these same species specialized for living in forested, karstic landscapes.

Fig. 8. Diagrammatic views contrasting adult skulls of Saxatilomys paulinae (Top, BMNH 2000.292, holotype) and Niviventer fulvescens (Bottom, AMNH 272365) from northern Vietnam.
Arrows indicate the different patterns formed by orientation of the squamosal root of the zygomatic arch. In S. paulinae, the ridge extending from the squamosal root meets the temporal ridge (formed along the squamosal-parietal suture) well anterior to the vertical ridge formed by the squamosal-exoccipital suture. In N. fulvescens and all other species of Niviventer, as well as Chiromyscus, the posterior extension of the squamosal zygomatic root parallels the temporal ridge to merge with the vertical ridge formed along the squamosal-exoccipital suture. Note also the much wider zygomatic plate of S. paulinae, another feature distinguishing that species from most other species of Niviventer. Scale line equals 10 mm.

ETYMOLOGY: We combine the Latin, saxatilis, meaning ‘‘among the rocks’’, with the Greek mys for mouse (or rat).

Saxatilomys paulinae, new species

ETYMOLOGY:During frequent and lengthy visits to the Natural History Museum in London over three decades, Musser (and probably other visitors) has forgotten how many times he sat on the front steps of that historical and hallowed building waiting for the guardians of the mammal collections to arrive and escort him in. But he has never forgotten the cheery morning greeting when Paula Jenkins arrived, the walk together to the office for the great ring of keys, and her courteous efforts to install him in storage rooms, making sure everything was available for another days work. We mammalian systematists have depended upon the mammal collections and library resources of the Natural History Museum for our research, and all of us came to depend upon Paula for access to the collections and for help with innumerable problems related to locating specimens, finding the critical gazetteers and

maps, and searching library shelves for publications and field journals. We also remember the times when she had to unlock the door to a collection room because we had inadvertently locked ourselves in. We are extremely pleased to honor Paula Jenkins by attaching her name to this beautiful, gray-furred rat that is part of the spectacular and unique limestone landscape in central Lao PDR.

Saxatilomys paulinaeMusser, Smith, Robinson & Lunde, 2005

Saxatilomys is a genus of Muridae rodent native to central Laos. It was first discovered in the Khammouan Limestone National Biodiversity Conservation Area in Khammouan Province. The name is derived from the Latin saxatilis, meaning "among the rocks" and the Greek mys meaning mouse or rat.

The genus is similar, and likely closely related, to the Niviventer and Chiromyscus genera. Saxatilomys is distinguished from these and other Indomalayan genera by "semispinous dark gray upperparts, dark frosted gray underparts, large, extremely bulbous footpads, and a combination of derived and primitive cranial and dental traits".

Musser, G.G., Smith, A.L., Robinson, M.F. & Lunde, D.P. 2005. Description of A New Genus and Species of Rodent (Murinae, Muridae, Rodentia) from the Khammouan Limestone National Biodiversity Conservation Area in Lao PDR. American Museum Novitates 3497: 1–31. DOI: 10.1206/0003-0082(2005)497[0001:DOANGA]2.0.CO;2

Most dromaeosaurids were small- to medium-sized cursorial, scansorial, and arboreal, sometimes volant predators, but a comparatively small percentage grew to gigantic proportions. Only two such giant “raptors” have been described from North America. Here, we describe a new giant dromaeosaurid,Dakotaraptor steini gen. et sp. nov., from the Hell Creek Formation of South Dakota. The discovery represents the first giant dromaeosaur from the Hell Creek Formation, and the most recent in the fossil record worldwide. A row of prominent ulnar papilli or “quill knobs” on the ulna is our first clear evidence for feather quills on a large dromaeosaurid forearm and impacts evolutionary reconstructions and functional morphology of such derived, typically flight-related features. The presence of this new predator expands our record of theropod diversity in latest Cretaceous Laramidia, and radically changes paleoecological reconstructions of the Hell Creek Formation.

Etymology.— Dakota, referring to the geographic location of the discovery as well as the Dakota First Nations Tribe, plus raptor, Latin for “plunderer”. The specific name honors paleontologist Walter W. Stein.

Locality and horizon.— Upper Hell Creek Formation (Upper Maastrichtian), no more than 20 m below the Cretaceous-Paleogene Boundary, Harding County, South Dakota, U.S.A. The fossils were discovered in medium- to fine-grained sandstone with clay-pebble laminae that was part of a low-energy stream channel facies. While the type strata were deposited in an active fluvial system, transport energy was sufficiently low that it was not uncommon to find bones >10 cm in length from various other taxa still articulated with their adjacent elements, and plant matter that bore virtually no taphonomic alteration. In several instances, articulated or associated small vertebrate skeletons were recovered. No other theropod bones were recovered from the type substratum except for Dakotaraptor. Flora at the study locality places the site within the HC III floral zone (Johnson, 2002).

Figure 4. Reconstructed Dakotaraptor wing and plumage, with avian and theropod comparisons. A, enlarged view of the quill knobs on the Dakotaraptor holotype ulna (PBMNH.P.10.113.T), compared with quill knobs in Velociraptor (B) and Concavenator (C); D, conservative reconstruction of the wing plumage for Dakotaraptor based on quill knob placement and comparison with other dromaeosaurid and bird wings; E, quill knobs on a modern Masked Booby (Sula dactylatra) ulna, and (F), X-ray of a modern Barred Owl (Strix varia) wing showing attachment of the remiges on the quill knobs. The flattened dorsal surface of Dakotaraptor’s metacarpal II would have provided a stable shelf for the primary remiges that laid across it, a possible driving force for evolving the flat surface.

A giant, feathered dromaeosaurid exhibited by gracile and robust morphotypes was unexpected and thus is an important addition to the Hell Creek fauna. It fills the gap in body size distribution between the small maniraptorans and large tyrannosaurids previously documented in the formation, while adding to the known diversity of Hell Creek maniraptorans. Dakotaraptor also records a fourth event in which dromaeosaurids achieved atypically large body size. Moreover, the presence of quill knobs, indicative of elongate, stiffened feathers on the forearms, is unprecedented in giant dromaeosaurids and requires a reexamination of trends in quill knob evolution. The functional morphology of the long feathers, possibly of modern avian aspect as implied by known Asian forms, must also be considered. Subsequent studies of Dakotaraptor and the Hell Creek fauna may aid in our understanding of the circumstances that prompted dromaeosaurids to retain ligamental architecture for feather attachment, and may also provide information critical to a more accurate understanding of the lost capacity for flight.

A team of researchers from the George Washington University and the Institut Català de Paleontologia Miquel Crusafont identified a new genus and species of small ape that existed before the evolutionary split of humans/great apes (hominids) and gibbons (the 'lesser apes' or hylobatids).

Miocene small-bodied anthropoid primates from Africa and Eurasia are generally considered to precede the divergence between the two groups of extant catarrhines—hominoids (apes and humans) and Old World monkeys—and are thus viewed as more primitive than the stem ape Proconsul. Here we describe Pliobates cataloniae gen. et sp. nov., a small-bodied (4 to 5 kilograms) primate from the Iberian Miocene (11.6 million years ago) that displays a mosaic of primitive characteristics coupled with multiple cranial and postcranial shared derived features of extant hominoids. Our cladistic analyses show that Pliobates is a stem hominoid that is more derived than previously described small catarrhines and Proconsul. This forces us to reevaluate the role played by small-bodied catarrhines in ape evolution and provides key insight into the last common ancestor of hylobatids (gibbons) and hominids (great apes and humans).

STRUCTURED ABSTRACT

INTRODUCTION

Reconstructing the ancestral morphotype from which extant hominoids (apes and humans) evolved is complicated by the mosaic nature of ape evolution, the confounding effects of independently evolved features (homoplasy), and the virtual lack of hylobatids (gibbons and siamangs) in the Miocene fossil record. For several decades, small-bodied anthropoid primates from Africa and Eurasia have not played an important role in this debate, because they generally lack the shared derived features of extant catarrhines (hominoids and Old World monkeys) and are thus considered to precede their divergence. Even some small-bodied catarrhines from Africa (dendropithecids), considered to be stem hominoids by some authors, are viewed as more primitive than the larger-bodied stem ape Proconsul. This has led to the assumption that hylobatids are a dwarfed lineage that evolved from a larger-bodied and more great ape–like common ancestor with hominids (great apes and humans).

RATIONALE

Here we describe a new genus of small-bodied (4 to 5 kg) ape from the Miocene (11.6 Ma), discovered in the Abocador de Can Mata stratigraphic series (Vallès-Penedès Basin, northeast Iberian Peninsula), that challenges current views on the last common ancestor of extant hominoids. This genus is based on a partial skeleton that enables a reliable reconstruction of cranial morphology and a detailed assessment of elbow and wrist anatomy. It exhibits a mosaic of primitive (stem catarrhine–like) and derived (extant hominoid–like) features that forces us to reevaluate the role played by small-bodied catarrhines in ape evolution.

Order: Primates

Suborder: Haplorhini

Superfamily: Hominoidea

Family: Pliobatidae Alba et al. 2015

Genus: Pliobates Alba et al. 2015

Species: Pliobates cataloniaeAlba et al. 2015

Reconstruction of the skull (front and side view) and representation of life appearance of Pliobates cataloniae are shown.

Long bones from the left arm of Pliobates cataloniae. Humerus (A), radius (B) and ulna (C).

photos: Institut Català de Paleontologia Miquel Crusafont (ICP)

RESULTS

The new genus retains some features that are suggestive of generalized above-branch quadrupedalism, but it possesses more extensive hominoid-like postcranial features (mostly related to enhanced forearm rotation and ulnar deviation capabilities) than those convergently displayed by atelids. Its overall body plan is more compatible with an emphasis on cautious and eclectic climbing, combined with some degree of below-branch forelimb-dominated suspension (although less acrobatic than in extant gibbons). Its relative brain size implies a monkey-like degree of encephalization (similar to that of hylobatids but below that of great apes), and dental microwear indicates a frugivorous diet. From a phylogenetic viewpoint, the new genus combines craniodental and postcranial primitive features (similar to those of dendropithecids) with multiple derived cranial and postcranial features shared with extant hominoids. Some cranial similarities with gibbons would support a closer phylogenetic link between the new genus and hylobatids. However, this possibility is not supported by the total evidence. A cladistic analysis based on more than 300 craniodental and postcranial features reveals that the new genus is a stem hominoid (preceding the divergence between hylobatids and hominids), although more derived than previously known small catarrhines and Proconsul.

CONCLUSION

As the first known Miocene small-bodied catarrhine to share abundant derived features with extant hominoids, the new genus indicates a greater morphological diversity than previously recognized among this heterogeneous group, and it provides key insight into the last common ancestor of hylobatids and hominids. Our cladistic results, coupled with the chronology and location of the new genus, suggest that it represents a late-surviving offshoot of a small African stem hominoid that is more closely related to crown hominoids than Proconsul is. These results suggest that, at least in size and cranial morphology, the last common ancestor of extant hominoids might have been more gibbon-like (less great ape–like) than generally assumed.

Representation of the environment and some of the species that inhabited the area of Els Hostalets de Pierola about 12 million years ago.

Apes are divided into two groups: larger-bodied apes, or hominoids, such as humans, chimps, and gorillas; and smaller-bodied hylobatids, such as gibbons. These two lineages are thought to have diverged rather cleanly, sharing few similarities after the emergence of crown hominoids. Alba et al. describe a new ape from the Miocene era that contains characteristics from both hominoids and small-bodied apes (see the Perspective by Benefit and McCrossin). Thus, early small-bodied apes may have contributed more to the evolution of the hominoid lineage than previously assumed.

The South American gymnophthalmid genus Euspondylus is distributed from Venezuela through Peru, with its highest diversity occurring in Peru.Euspondylus paxcorpus sp. nov. is a new species from Junín, Peru possessing prefrontal scales and represented by 60 specimens. The new species differs from all other species by the combination of four supraoculars with supraocular/supraciliary fusion, 5–7 occipitals, a single palpebral scale, five supralabials and infralabials, quadrangular dorsal scales with low keels arranged in transverse series only, 40–45 in a longitudinal count and 22–28 in a transverse count, 12 rows of ventrals in a transverse count and 23–25 in a longitudinal count, and no sexual dimorphism in coloration. The discovery of E. paxcorpus increases the known number of Euspondylus species to 13. Because the coloration patterns of the specimens were greatly different after preservation in alcohol, caution should be used when identifying Euspondylus species from museum specimens.

Distribution and natural history.Euspondylus paxcorpus is endemic to the eastern slope of the Cordillera Oriental of the central Peruvian Andes. All specimens were collected by day associated with groups of rocks near small farms between 3500–3800 masl in the district of Ulcumayo, region of Junín, Peru. The terrain is montane and andenes (agricultural terraces) constructed by the local pre-hispanic culture dominate the area and have been maintained for the continued cultivation of potatoes (Solanum spp.), olluco (Ullucus tuberosus), oca (Oxalis tuberosa), mashua (Trapaeolum tuberosum), and fava beans (Vicia faba). The climate is defined as boreal (Dwb, Köppen–Geiger climate classification system) and is cold and dry with a marked difference between day and night (approximately 7 to 15 ̊C difference) stereotypical of the Suni and Quechua natural regions (Monge Miguel et al., 1996). An intense rainy season occurs between the months of December and March. The flora is mainly composed of small herbaceous plants and grasses including Jarava ichu. The only other reptile species found in the area was the dipsadid snake Tachymenis peruviana Wiegmann. Interestingly, in the district of Ulcumayo and surrounding areas, E. paxcorpus is used for traditional medicinal purposes; specimens are flayed and tied to extremities to heal broken bones. The use of reptiles for medicinal means is not limited to E. paxcorpus in Ulcumayo, as snakes are commonly left to steep in sugar cane alcohol called cañaso and considered a curative. In Quechua these lizards are referred to as shakurhuay.

Etymology. The specific epithet paxcorpus is a Latin noun that honors the Peace Corps, or Cuerpo de Paz in Spanish. The lizards were discovered and collected by a Peace Corps Volunteer during his service in Peru to promote community-based environmental management.

Discussion

The description of Euspondylus paxcorpus brings the current number of Euspondylus species to 13. In Peru nine or 10 species occur (it is questionable whether E. guentheri occurs in Peru), with three other species (E. josyi, E. maculatus, and E. spinalis) also occurring within the Junín region, though none of them is sympatric with E. paxcorpus. In fact, although E. paxcorpus was quite abundant in all areas where it was located, no other lizard species were found locally.

One striking finding during this study was the drastic difference in coloration of all specimens from life to after preservation in ethanol (Fig. 3). In ethanol, all specimens had a uniform dark brown dorsum, head, and dorsal surface of the tail, with no stripes, spots, or variations in color visible. However, the coloration in life showed visible spots, ocelli, stripes, and different regions of color. These differences do not bode well for the examination of museum specimens of Euspondylus or other species whose coloration is so greatly altered. In our experience, though colors typically fade in alcohol, patterns are usually still visible in other species. The fact that no patterning is visible indicates that the examination of color patterns of museum specimens may give misleading information about the coloration of living specimens and conclusions about coloration based solely on museum specimens should be treated with caution.